ORIGINAL ARTICLE
Benign Papillomas Diagnosed on Large-gauge
Vacuum-Assisted Core Needle Biopsy which Span
<1.5 cm Do Not Need Surgical Excision
Andrew D. Mosier, DO,* Joren Keylock, MD,† and Donald V. Smith, MD‡
*Cleveland Clinic Foundation Imaging Institute, Cleveland, Ohio; †Department of Pathology,
St. Claire Hospital, Lakewood, Washington; ‡Department of Radiology, Madigan Army Medical
Center, Tacoma, Washington
n Abstract: The objective of our study is to determine if a carefully selected subset of benign breast papillomas (size
≤1.5 cm) can be safely followed by imaging surveillance instead of immediate surgical excision. Over a 6½-year period, 86
breast lesions were diagnosed as a benign papilloma (BP) utilizing an 11- or 8-gauge vacuum-assisted core needle biopsy
(VACNB) device. In general, it was our intent to remove as much of the radiologically evident lesion as possible. These 86
lesions underwent ≥2 years of imaging surveillance, without surgical excision following initial detection. With ≥2 years of
radiologic follow-up, none of the 86 BPs demonstrated imaging findings that necessitated repeat biopsy or surgical excision.
Benign breast papillomas ≤1.5 cm that are biopsied using an 11- or 8-gauge VACNB device with intent to remove as much
of the radiologically evident lesion as possible are safe to undergo serial imaging surveillance rather than immediate surgical excision. n
Key Words: benign papilloma, intraductal papilloma, papilloma excision
A
papillary lesion of the breast is a general descriptor for a continuum of benign to malignant
lesions, which include benign papillomas (BP), papillomatosis and sclerosing papillomas, atypical papillomas, micropapillary ductal carcinoma in situ (DCIS),
and papillary breast carcinoma or invasive ductal carcinoma (IDC) (1,2). Papillary breast carcinoma itself
accounts for only about 2% of all breast cancers (3).
Despite this distinct terminological continuum of papillary lesions, it can be difficult to differentiate borderline lesions (i.e., atypical papilloma versus papillary
carcinoma) on the basis of histopathologic features. In
the past, this challenge has made certain difficult cases
arbitrarily subjective for the interpreting pathologist
(2,4).
Address correspondence and reprint requests to: Andrew D. Mosier,
The Cleveland Clinic Foundation Imaging Institute, 9500 Euclid Ave/A-10,
Cleveland, OH 44195, USA, or e-mails: [email protected]; andrew.d.
[email protected]
Disclaimer: The views expressed are those of the author(s) and do not
reflect the official policy of the Department of the Army, the Department of
Defense or the U.S. Government.
DOI: 10.1111/tbj.12180
© 2013 Wiley Periodicals, Inc., 1075-122X/13
The Breast Journal, Volume 19 Number 6, 2013 611–617
The difficulties in management and disposition of
papillary breast lesions begin with the physician who
performs the biopsy. Sampling error leading to a falsenegative result is often cited as the foremost reason to
excise all papillary lesions diagnosed by fine-needle
aspiration (FNA) and smaller gauge core needle
biopsy (CNB). These sampling methods may miss
areas of atypia or small malignant foci (3,5–9). Pathologic distinction may remain difficult even with biopsy
of the entire lesion, particularly when the lesion is not
reviewed by a pathologist subspecialized in breast disorders (1,2,10).
More recently, studies have suggested that surgical
excision may not be necessary for accurate diagnosis
of benign papillary lesions sampled by larger (11- or
8-gauge) VACNB devices and confirmed as benign by
surgical excision (3,11), 2-year imaging follow-up, or
a combination of both (12,13).
In our study, the reliability of imaging surveillance
for BPs ≤1.5 cm initially sampled with an 11- or
8-gauge VACNB device was retrospectively assessed
over a 6½-year period at our institution. BPs greater
than 1.4 cm tend to be malignant more often than those
which were smaller (1); and no papillary lesion we
assessed (whether by mammography, ultrasound, or
612 • mosier
ET AL.
final pathology) was >1.5 cm. In general, it is our practice to remove as much of the radiologically evident
lesion as possible (whether calcifications and/or a mass
with stereotactic technique, or a mass with ultrasoundguided biopsy technique). Of note, a predecessor study
at our institution by Sohn et al. (14) retrospectively
assessed the upgrade rate of papillary breast lesions
sampled by 14- or 11-gauge biopsies from January
1994 to December 2005. Sohn et al. found that only
two lesions initially designated as BP (1.1%) were
upgraded (to carcinoma) following surgical excision.
MATERIALS AND METHODS
Subjects
We reviewed all BPs at our institution from January
2003 to June 2009. January 2003 was designated as
our starting point because this is when we began more
routine use of our 8-gauge VACNB biopsy device. June
2009 was designated as the end point to give ≥2 years
for possible follow-up imaging surveillance (assuming
patients would return as scheduled). This end point
was additionally chosen because 2 years is the time
interval used to more closely follow a probably benign
finding until it can be reduced from a Breast ImagingReporting and Data System (BI-RADS) 3 to BI-RADS
2. During this time, 4293 CNBs were performed.
For inclusion into the study, all papillary lesions
were confirmed as a BP following initial sampling by
an 11- or 8-gauge VACNB intended to remove as
much as possible of the sonographically visible lesion
or stereotactically visible calcifications. On average,
visible lesional removal required four samples with an
8-g VACNB device, and six to seven with and 11-g
VACNB device. These BP then demonstrated benign
radiographic findings for at least 2 years on follow-up
mammograms, without change necessitating repeat
biopsy or surgical excision. In most cases, follow-up
consisted of mammograms every 6 months for
2 years, and then annually thereafter.
One hundred and fifty-two papillary lesions were
identified by an 11- or 8-gauge VACNB. Of these, 11
papillary lesions (7.1%) were associated with atypia
(PA) and 12 (7.7%) with malignancy (PM). These 23
PAs and PMs were excluded because it is standard of
care to recommend surgical removal for all PAs and
PMs. Ten BPs were surgically excised after VACNB
due to patient preference, and were therefore excluded
from the study (even though these 10 were confirmed
as BPs following surgery). Finally, one papilloma was
excluded because it was initially designated a BIRADS five lesion, requiring surgical excision. The
surgical specimen revealed a final diagnosis of a BP.
Fifteen BPs have not yet completed 2 years of imaging
follow-up (either due to patient noncompliance; or
because the patient has not yet completed a follow-up
mammogram at least 2 years from the excision date).
These 15 have therefore been excluded. In addition,
17 have been lost to follow-up prior to 2 years of
imaging follow-up, mostly due to patient relocation.
Thus, these 17 have also been excluded.
Eighty-six BPs (in 84 women; two women had multiple BPs) remained following the aforementioned
exclusions. The average age of the patient at the time
of biopsy was 54 years 6 months (range of 32.9–
83.1). The average length of radiographic follow-up
(from initial biopsy to the most recent examination
reconfirming a benign appearance) is 4 years
10 months (range of 2–8.83 years), with 41/86 lesions
above this average length of follow-up time.
Overall, only 45 of 86 BPs were initially radiologically evident by mammography as a mass/focal
asymmetry with (8) or without (37) suspicious microcalcifications. The remaining 41 BPs were incidentally
discovered in the management of suspicious microcalcifications (29), bloody nipple discharge (5), a palpable abnormality (5), or on the preoperative MRI of a
contralateral breast cancer (2).
Management and Follow-up
Thirty-seven BPs were initially discovered on mammography as a mass or focal asymmetry without associated calcifications. All 37 of the BPs were next
imaged with ultrasound, which redemonstrated the
mammographically evident mass in 35 of 37. These
35 BPs were biopsied with ultrasound guidance. The
other two BPs not visualized by ultrasound underwent
biopsy with stereotactic guidance.
Eight BPs were initially discovered on mammography as a mass/focal asymmetry with associated microcalcfications. All eight were next imaged with
ultrasound, which redemonstrated the mass in seven
of the eight. Five of the eight underwent stereotactic
biopsy (including the one BP, which did not show an
associated mass on ultrasound). The other three BPs
were biopsied with ultrasound guidance because the
sonographic mass was more obvious than the mammographic calcifications.
Alternate Management of Benign Papillomas • 613
Twenty-nine BPs were initially discovered on mammography as microcalcifications without an associated
mass or asymmetry. Because there was no associated
mass or asymmetry, and because 0 of the 29 patients
reported a palpable lesion, ultrasound was not performed. All 29 underwent stereotactic 11- or 8-g
VACNB.
Five BPs were initially discovered on ultrasound as
part of the management for a clinically palpable mass.
Five other BPs were first discovered on US (2) or MRI
(3) as part of the management for bloody nipple discharge. All 10 of these BPs underwent ultrasoundguided VACNB. We generally evaluate bloody nipple
discharge with MRI and mammography—often with
additional MR-directed (or 2nd-look) ultrasound
when appropriate. The three BPs associated with
bloody nipple discharge [initially discovered on MRI]
were subsequently confirmed on a MR-directed ultrasound exam prior to ultrasound-guided VACNB.
Two BPs were initially discovered as small masses
on preoperative MRI in the management of a contralateral breast cancer. They were subsequently confirmed on MR-directed ultrasound. Next, they
underwent ultrasound-guided VACNB and were confirmed as BPs. To date, both remain unchanged in
their mammographic appearance.
When the BPs of this study were biopsied with
ultrasound guidance (and the percentage removed was
included in the postprocedure report by the radiologist), no less than 75% and no more than 90% of
the radiographically evident lesion was reportedly
removed. Often because of location (retroareolar,
Figure 1. Initial (left), 6-month follow-up
(middle), and 3-year follow-up (right) craniocaudal views of the left breast demonstrate a
nonspecific mass (white circle) in the upperouter quadrant of the left breast (bracketed
by the black oil pencil). The mass on the
initial mammogram was excised and a clip
was placed. The mammographic appearance
remained benign without development of
suspicious calcifications or a mass at or
adjacent to the biopsy site.
within a dilated duct) and/or clinical history (bloody
nipple discharge), we had a high degree of suspicion
before the biopsy that the mass may be a BP.
However, when the BPs of this study were biopsied
with stereotactic guidance for a cluster of suspicions
microcalcification, we often did not suspect that the
suspicious microcalcifications were possibly caused by
a BP prior to biopsy. Therefore, when stereotactic
biopsy of suspicious grouped or clustered calcifications
is performed, it is our practice to remove most (>75%)
to all of the radiographically evident calcifications.
However, we do not routinely report a percentage or
estimation of calcifications removed. Nor do we reposition the stereotactic biopsy needle unless absolutely
necessary (for reasons beyond the scope of this paper)
if calcifications are adequately obtained within the
biopsy specimen on specimen mammography.
After each biopsy (ultrasound-guided or stereotactic), a clip is placed, and a postprocedure mammogram is obtained. We do not routinely review biopsy
margins with pathology. Instead, follow-up mammograms are obtained every 6 months for 2 years, and
annually thereafter.
Mammographic images of a BP, and its typical
appearance on multiple follow-up images, have
been included below (Fig. 1). There is no growth/
development of a new mass or suspicious calcifications
at or adjacent to the clip (biopsy site) over the course
of the follow-up images. In addition, ultrasound
(Fig. 2), MRI/US (Fig. 3), and implant/implantdisplaced mammograms (Fig. 4) of BPs are presented
for review.
614 • mosier
ET AL.
Figure 2. Grayscale (left) and color Doppler (right) ultrasound images of the left breast demonstrate a hypoechoic, retroareolar 8–9 mm
mass in a dilated duct with a mild amount of blood flow. The mass has the usual location and appearance of a benign papilloma (BP). This
mass underwent an 8-g vacuum-assisted core needle biopsy and was confirmed as a BP.
Figure 3. Longitudinal ultrasound (top left)
of the left breast demonstrates an isoechoic
mass (white arrowhead) attached to a slender pedunculated stalk (white circle) within a
dilated duct. MR (Siemens 3.0 T, prone) T1
postcontrast with fat saturation (top right;
sagittal, 20 cc IV Magnevist, TR 4, TE 1.4,
ST 1), T1 (bottom left; axial, TR 6.7, TE
2.63, ST 1.5), STIR (bottom right; axial, TR
6040, TE 63, ST 3) demonstrates an
enhancing mass (white circle) attached to the
slender pedunculated stalk (white circles on
T1 and STIR) within a dilated duct. Following
8-g vacuum-assisted core needle biopsy, the
imaging findings were confirmed as a pedunculated, intraductal papilloma.
Procedure
An 8- or 11-gauge VACNB device (Mammotome;
Ethicon Endo-Surgery, Cincinnati, OH) was used for
both ultrasound-guided and stereotactic biopsies. Preference was given to the 8-gauge biopsy device with
intent to remove as much of the lesional calcifications
(stereotactic approach) or mass (ultrasound or stereotactic approach) as possible. An 8-gauge needle was
also preferred when possible to retrieve a larger histologic sample per core, and for more complete sampling of the lesion. Exceptions to our preference for
the 8-gauge system were made in the following
instances: 1—the lesion was too close to the skin surface; 2—compression was not adequate for stereotactic
technique leading to a negative stroke margin; or
3—color Doppler demonstrated abundant vascularity
or a large vessel adjacent to the lesion (to mitigate the
risk of a hematoma).
RESULTS
To date, 0 of the 86 BPs that have undergone at
least 2 years of benign mammographic follow-up have
demonstrated change on imaging that would necessitate repeat biopsy or surgical excision. We did
encounter one case of interest where the patient
underwent a mastectomy for DCIS in a different
quadrant from a BP identified 4 years earlier in the
same breast. The clip of that BP was 5.0 cm from the
Alternate Management of Benign Papillomas • 615
Figure 4. Implant (left) nondisplaced, craniocaudal mammographic views of the right
breast obscure a subtle mass. The triangular
marker represents a palpable abnormality.
Implant-displaced, craniocaudal views (middle) confirm a mass at the site of the palpable abnormality. This mass was biopsied and
confirmed as a benign papilloma. Nine
months later, the patient returned for followup imaging (right, CC view of the right
breast) and no residual mass is visualized at
the site of the biopsy (clip).
closest margin of the intermediate-grade DCIS on final
pathology, and no atypia or malignancy was identified
at or adjacent to the clip.
The average size of the 86 BPs (when reported) was
7.5 mm (n = 49; range of 3–15 mm). The average
number of cores was 6.6 (range: 2–18) for 11-gauge
biopsies, and 4.33 (range: 1–8) for 8-gauge biopsies.
Forty-four biopsies (51.2%) were performed with an
11 gauge device; 27 by US-guidance and 17 by stereotactic technique. Forty-two (48.8%) biopsies were performed with an 8 gauge device; 26 by US-guidance
and 16 by stereotactic technique. Fifty-six papillomas
were located in the left breast and 30 in the right
breast.
DISCUSSION
Because many papillary lesions are undetected [as a
discrete mass] on mammography, differentiation by
imaging alone has previously proven unreliable (15);
however, a newer study notes that certain sonographic
features suggest benignity. Benign papillary lesions
tend to demonstrate homogeneous echotexture, in
contrast to malignant or high-risk lesions, which often
demonstrate mixed or complex cystic echogenicity. In
addition, benign papillary lesions were more often
well-circumscribed when compared with malignant
equivalents. Finally, no benign papillary lesion demonstrated angular margins or spiculation (3).
Multiple additional confounding variables must be
considered. It has been postulated that papillomas
may be a precursor of papillary carcinoma; or that
they may degenerate into a malignant lesion over
time (1,10,14,16). Also, a carcinoma in situ [PM]
diagnosed by CNB may be upgraded to invasive cancer when the entire lesion is examined (17–20).
These observations, however, were based on results
from smaller gauge core biopsy without vacuum
assistance; and without [expressed] intent to remove
as much of the radiographically evident lesion as
possible. It is indeed known that CNB without vacuum assistance has been associated with significantly
higher false-negative rates and histologic upgrade
than biopsies performed with vacuum assistance. The
aforementioned studies are also reporting the upgrade
rate of PA and PM, which we always recommend
for surgical excision and have therefore excluded
from our study. Moreover, more recent studies suggest that histologic upgrade from lesional undersampling is not as prevalent with VACNB as previously
suggested (13).
A recent study by Chang et al. correlates the size of
a benign papillary lesion with its potential for histologic upgrade to carcinoma. As may be expected,
malignancies tended to be larger (average of 1.4) than
benign lesions (average of 0.9 cm) (1). However, we
did not have a benign papillary lesion greater than
1.5 cm in our sample group, and the average size of
papillary lesions in our study was around 7.5 mm.
As recently as 2008, the surgical literature reported
that all papillomas require surgical excision regardless
of radiologic–pathologic correlation when utilizing a
14-gauge CNB technique (21). In that same year, a
similar conclusion was suggested by Shin et al.
616 • mosier
ET AL.
Regardless of the somewhat inconsistent nature of recommended follow-up for benign papillary lesions, it is
the accepted standard of care to excise all papillomas
with any degree of atypia or malignancy (14,22,23).
Chang et al. affirmed that surgical excision is required
for accurate diagnosis of papillary lesions sampled by
CNB (1); however, a more recent paper by the same
author suggests that surgical excision may not be necessary when these lesions are sampled by an 11-gauge
US-guided VACNB device (11). A recent article by
Kim et al. also challenges the recommendation for
surgical excision, as this study demonstrated a 0%
upgrade rate to carcinoma in 54 BPs initially biopsied
by an 11- or 8-gauge VACNB technique. Kim et al.
has also followed a large number of initially BPs that
were not immediately excised and remained radiographically benign without changes necessitating surgical excision (13).
Some studies have reported that BPs demonstrating
radiologic–pathologic concordance can be safely
observed with mammographic follow-up (22,24,25).
In 2008, Kim et al. reported that surgical excision is
not necessary for accurate diagnosis in a series of 39
papillary lesions removed by 11- or 8-gauge
US-guided vacuum-assisted technique (12).
What is becoming clear is that sampling error is
significantly reduced with increased core needle gauge
size (11–13), vacuum assistance (3), and intent to percutaneously remove most or all of the visualized lesion
(12). Furthermore, the use of an 8-gauge VACNB to
achieve lesion removal appears to circumvent the need
for subsequent excision (12), particularly when the
lesion demonstrates benign findings on follow-up for
≥2 years (22) (Table 1).
A few limitations of our study merit consideration.
The sample size was affected by 17 patients who were
lost to follow-up (usually due to patient relocation). A
second limitation is lack of definitive radiologic–pathologic correlation, as none of the 86 BPs included in
the study has undergone surgical excision for histologic confirmation. Indeed, BPs subjected to surgical
excision could have represented a control group for
the study, allowing for true statistical analysis of BPs
diagnosed by VACNB at our institution. However,
because 24 months of serial imaging is required to
reassign a BI-RADS 3 (probably benign) lesion to
BI-RADS 2 (benign), it is unlikely that a surgically
excised control group would change the management
or categorization of these lesions as the average follow-up time of the BPs we reviewed is 58 months.
Finally, even though the 86 BPs in this study are the
largest current [reported] group of BPs followed exclusively by imaging, an even greater number of BPs
would have allowed for greater levels of assurance.
Our data suggest that at 2 years post biopsy, there
is no difference in the outcome of BPs initially biopsied by a large-gauge VACNB and closely followed by
imaging surveillance, versus those which are immediately surgically excised. Therefore, BPs less than
1.5 cm, biopsied by 11- or 8-g CNB, using vacuum
assistance, with intent to remove as much of the
radiographically-evident lesion as possible, do not
require immediate surgical excision if instead followed
by short-interval imaging surveillance. The radiographic follow-up of BPs should, therefore, be a focus
of future interest as the cost, risk, and morbidity of
surgical excision can potentially be avoided.
LEARNING POINTS
1 All papillary lesions with atypia and malignancy
should undergo surgical excision.
Table 1. Summary of Recent Studies on Management of Papillary Breast Lesions
Study
Kim et al. (13)
Chang et al. (1)
Chang et al. (11)
Shin et al. (3)
Kim et al. (12)
Sydnor (22)
Number of papillary lesions
upgraded after surgical excision
14 g – 12 of 157 (7.6%)
11 and 8 g – 0 of 54 (0%)
14 g – 8 of 54 (14.8%)
11 g – 0 of 10
11 and 8 g – 3 of 49 to
atypical (6.1%), 0 to malignancy
11 and 8 g – 2 of 15 (13.3%)
to atypical, and 2 to malignancy
11 g – 0 of 29 (0%)
8 g – 0 of 10 (0%)
14 and 11 g – 1 of 38 (2.6%)
Conclusion
Surgical excision may not be mandatory for benign papillary lesions removed by US-guided
VACNB
Surgical excision is required for accurate diagnosis of benign papillomas removed by CNB
Surgical excision may not be required for benign papillomas removed by 11-gauge
US-guided VACNB
Surgical excision should be performed for accurate diagnosis of papillary lesions
Surgical excision may not be required for benign papillary lesions excised by US-guided
directional vacuum-assisted removal
Mammographic follow-up is reasonable for a benign papilloma diagnosed at core biopsy
based on an infrequent (3%) association of this lesion with cancer
Alternate Management of Benign Papillomas • 617
2 Papillary lesions eligible for mammographic follow-up (instead of surgical excision) include those
which meet all of the following criteria:
• a papillary lesion less than 1.5 cm on initial
radiographic imaging (measured if visualized as
a mass on mammogram or ultrasound);
• biopsied by a large-gauge (11 or 8 g), vacuumassisted, core needle biopsy device; and
• confirmed as a BP by pathology.
3 Typically, follow-up should include a mammogram
every 6 months for the first 2 years, and annually
thereafter.
4 Any concerning mammographic change (increasing
calcifications or new/recurrent mass at the site of the
biopsy clip) should prompt a full re-assessment and
discussion of surgical excision even if a repeat biopsy
is benign.
5 When following over 86 BPs with the criteria from
learning points 1–3, 0 of the 86 BPs have demonstrated any change necessitating repeat biopsy or surgical excision with an average of 58 months of benign
imaging follow-up.
CONFLICTS OF INTEREST
None.
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